The soybean aphid, Aphis glycines Matsumura, is a newly invasive insect species that seriously threatens U.S. soybean production. It is the only aphid species to develop large colonies on soybeans, Glycine max, in North America. Since its first appearance in Wisconsin, it has spread to over 20 states in the U.S. and three provinces in Canada (Soybean Aphid Watch 2005). Infestations of this pest whittle soybean growers' profits and cause hundreds of millions of dollars in losses (CNN News, Nov. 25, 2003; Chicago Tribune Business News, Oct. 11, 2003). In 2003, the total acreage having soybean aphid infestations was estimated at over 8 million acres, with yield losses ranging from 32%-45% from the three biggest soybean-growing states (data digested from research conducted in Illinois, Iowa and Minnesota and reported at the Midwest Soybean Aphid Workshop, Feb. 5, 2004).
The soybean aphid is originally a native of China and Japan, and until recently, mainly occurred only in several Asian countries, Australia, and on several Pacific islands. It has a complex life cycle with more than 15 generations annually. Two different types of host plants are necessary for the completion of its life cycle. In Iowa, winter survival of overwintering eggs occurs on the aphid's primary host, the common buckthorn, Rhamnus cathartica. However, winged females (called ‘gynoparae’) are also found on the leaves of another Rhamnus species (R. alnifolia) in other north central states (Voegtlin et al., 2004). The gynoparae produce a generation of wingless pheromone-emitting females (called “oviparae”) in late fall on buckthorn. This is the only sexually reproducing generation, and the only one in which sex pheromones are used for mating. The overwintering eggs from these wingless females that mate with winged males in the fall result in the first winged generation (alate viviparous female) that take flight early in the spring. These females migrate from buckthorn in search of soybeans, Glycine max, the secondary host plant. On soybeans, a series of wingless generations (apterous viviparous females) are produced, which are followed by a winged generation that disperses from infested soybean plants in search of other less-infested soybean plants. During the fall, winged females (gynoparae) fly back to the common buckthorn to produce a new generation of pheromone-producing oviparae. Males that develop late in the season on soybeans search for buckthorn and mate with oviparae, which lay the overwintering eggs on buckthorn twigs (See FIG. 1, diagram of the soybean aphid life cycle).
Application of insecticides has been the first approach to suppress this pest species during the growing season, but there are the usual risks that beneficial insects will be killed or repelled and that the environment can become polluted. Furthermore, insecticides may not be entirely effective, and populations of soybean aphids do tend to rebound after insecticide application by developing resistance quickly (Cullen, 2004; Ostlie, 2004). The insecticides labeled for soybean aphid management listed in Table 1 are all restricted from use within at least 20 days of harvesting by the EPA; this is the most critical period of the life cycle, during which the overwintering population is generated. Further results from soybean aphid suction traps during the fall of 2002 have shown that the higher density fall population in 2002 contributed to the most serious soybean aphid infestation during 2003 since the arrival of this in the U.S. (Voegtlin and Steffey, 2004).
TABLE 1Insecticides Labeled for Soybean Aphid ControlRatePost HarvestInsecticide(fl oz/acre)Restriction (day)ClassAsana XL5.8-9.621PyrethriodBaythroid 2E2.845PyrethriodDimethoate1621OrganophosphateFuradan 4F821CarbamateLorsban 4E16-3228OrganophosphateMustang Max3.4-4.321PyrethriodPenncap-M32-4820OrganophosphatePounce 3.2EC4-860PyrethriodWarrior T1.92-3.8445Pyrethriod
During the growing season, soybean aphids are attacked by a variety of insect predators and parasitoids. The complex of these natural enemies plays a potential key role in regulating soybean aphid populations. Field observations in soybean fields indicate that Coccinella septempunctata dominates early in the season with an increasing abundance of Harmonia axyridis and Coleomegilla maculata as the season progresses. The most common lacewing species, Chrysoperla carnea, also flies during the soybean growing season, and their larvae have been observed attacking soybean aphids. There is also an abundance of larvae of syrphid flies preying on soybean aphids. We documented a second lacewing species, Chrysopa oculata, flying in the late fall when gynoparae and sexually active male and female soybean aphids occur. These lacewings are predacious during both the adult and larval stages. The inventors here isolated and identified several plant-related volatile compounds that attract the adults of several species of predaceous insects (Zhu et al., 2005; Zhu and Park, 2005).
The use of predaceous insects, including coccinellids, chrysopids and other predatory insects, as biological control agents to suppress population of pest species on economically important agricultural crops or in home gardens, is widely accepted and recognized by the general public and by biological control practitioners (see references in, Obrycki and Kring, 1998; Canard, et al 1984). There have been significant successes in using such insects to suppress whitefly, aphid, mealybug, scale and mite populations (Gerling, 1990; Frazier, 1988; New, 1975). Despite the significant success of employing these two groups of predatory insects for biological control, two of the most important factors impacting the effectiveness of biological control are the timing of the abundance of predatory insects on targeted pests and the dispersal behavior of many predaceous species (Frazier, 1988; Rutledge et al. 2004). The use of attractants of predatory insects of soybean aphids offers significant potential to manipulate these beneficial insects in aphid-infested habitats (Zhu et al., 1999; Zhu et al., 2005; Zhu and Park, 2005).
During the fall, gynoparae fly from soybean fields to locate their winter host plants, where they give birth to live, wingless, sexually-active females (oviparae). These females are the only sexually reproducing females during the entire year. The mature oviparae emit a sex pheromone that attracts winged males from the same generation that produced the gynoparae; these males have also flown out of soybean fields to locate buckthorn plants. The eggs resulting from mated oviparae are laid on buckthorn for overwintering. The sex pheromone is released from glandular cells on the tibiae of the hind legs; this communication system has been demonstrated in several aphid species (Pettersson, 1970 and 1971, Pickett et al., 1992).
The sex pheromones of several aphid species that have been identified thus far (Picket et al., 1992; Boo et al., 2000) all involve compounds derived from the catmint plant, Nepata cataria. These include two compounds, (1R,4aS,7S,7aR)-nepetalactol (nepetalactol) and (4aS,7S,7aR)-nepetalactone (nepetalactone), the precise blend of which we determined specifically attracts both spring alatae and males and gynoparous soybean aphids (Zhu et al., submitted).
The aphid olfactory receptor system shows a great abundance of organs called secondary rhinaria that are located on the antenna of the alate morphs. The majority of these rhinaria are flat, plate-like organs (placoid sensilla) (Anderson and Bromley, 1987), which suggests their involvement in host plant location and mate finding (Eisenbach and Mittler, 1980; Marsh, 1975; Pettersson, 1971). In soybean aphids, Du et al. (1995) reported that the olfactory systems of soybean aphid males and gynoparous females are quite similar with regard to the abundance of placoid sensilla found on their antennae.
The use of synthetic sex pheromone to disrupt mating behavior has become a widely accepted and increasingly used IPM tool for suppressing populations of several key lepidopteran pests of agricultural crops and tree fruits around the world (Baker and Heath, 2004; Baker et al., 1997; Sanders, 1997). These disruption systems have resulted in a significant reduction in the number of insecticide applications (Baker and Heath, 2004; Staten et al., 1990; Baker et al., 1990). Earlier reports have suggested that the active range of male aphids responding to female sex pheromone is relatively short, which could be problematic when developing mating disruption techniques against aphid pests. However, recent studies have shown that males of several aphid species can be selectively attracted to traps releasing synthetic aphid pheromones at relatively long distances, as can gynoparous female aphids be attracted to host plant associated volatiles (Campbell et al., 1990; Hardie et al., 1992; 1996; Boo et al., 2000; Lösel et al., 1996a, b). These recent findings are encouraging for the potential deployment of aphid mating disruption technique using sex pheromones.
Another integrated pest management (IPM) component, mass trapping of insect pests using sex pheromones or host plant volatiles, has also shown renewed promise as a population management tool (Kobayashi et al., 1981; Smit et al., 2001) for both moth and beetle pests (Baker and Heath, 2004). Mass trapping of male soybean aphids as they leave soybean fields to locate females on the winter host, by using inexpensive traps placed in soybean fields, may be a feasible approach to explore. Likewise, mass trapping of gynoparae leaving soybean fields may reduce population densities of overwintering aphids.
There is a particular need to identify such compounds for use in suppressing and impacting soybean aphid populations, a pest causing economic damage.